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Antibodies and Superantibodies in Patients with Chronic Rhinosinusitis with Nasal Polyps

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Antibodies and Superantibodies in Patients with Chronic Rhinosinusitis with Nasal Polyps Antibodies and superantibodies in patients with chronic rhinosinusitis with nasal polyps Jiun-Bo Chen, PhD,a,b Louisa K. James, PhD,a,c Anna M. Davies, PhD,a,c Yu-Chang Bryan Wu, PhD,a,c Joanne Rimmer, FRCS,d Valerie J. Lund, MS, FRCS,d Jou-Han Chen, MS,b James M. McDonnell, PhD,a,c Yih-Chih Chan, PhD,a,c George H. Hutchins, BSci,a Tse Wen Chang, PhD,b Brian J. Sutton, DPhil,a,c Harsha H. Kariyawasam, FRCP, PhD,d and Hannah J. Gould, PhDa,c London, United Kingdom, and Taipei, Taiwan Background: Chronic rhinosinusitis with nasal polyps is basophil degranulation, and IgG1 or antigen-binding associated with local immunoglobulin hyperproduction and the fragments of each anti-SEE enhanced degranulation by the presence of IgE antibodies against Staphylococcus aureus other anti-SEE. enterotoxins (SAEs). Aspirin-exacerbated respiratory disease is Conclusions: SEEs can activate basophils by simultaneously a severe form of chronic rhinosinusitis with nasal polyps in binding as antigens in the conventional manner to CDRs and as which nearly all patients express anti-SAEs. superantigens to framework regions of anti-SEE IgE in Objectives: We aimed to understand antibodies reactive to anti-SEE IgE-FcεRI complexes. Anti-SEE IgG1s can enhance SAEs and determine whether they recognize SAEs through the activity of anti-SEE IgEs as conventional antibodies through their complementarity-determining regions (CDRs) or CDRs or simultaneously as conventional antibodies and as framework regions. ‘‘superantibodies’’ through CDRs and framework regions to Methods: Labeled staphylococcal enterotoxin (SE) A, SED, and SEEs in SEE–anti-SEE IgE-FcεRI complexes. (J Allergy Clin SEE were used to isolate single SAE-specific B cells from the Immunol 2016;nnn:nnn-nnn.) nasal polyps of 3 patients with aspirin-exacerbated respiratory Key words: disease by using fluorescence-activated cell sorting. Chronic rhinosinusitis with nasal polyps, aspirin-exac- Recombinant antibodies with ‘‘matched’’ heavy and light chains erbated respiratory disease, Staphylococcus aureus enterotoxin, superantigen, superantibody, basophil were cloned as IgG1, and those of high affinity for specific SAEs, assayed by means of ELISA and surface plasmon resonance, were recloned as IgE and antigen-binding fragments. IgE activities were tested in basophil degranulation assays. Staphylococcus aureus and its superantigens are implicated in Results: Thirty-seven SAE-specific, IgG- or IgA-expressing the intense inflammatory processes of the upper and lower air- 1 B cells were isolated and yielded 6 anti-SAE clones, 2 each for ways in patients with allergic diseases. These superantigens, SEA, SED, and SEE. Competition binding assays revealed that in particular Staphylococcus aureus enterotoxins (SAEs), are the anti-SEE antibodies recognize nonoverlapping epitopes in strongly associated with chronic rhinosinusitis with nasal polyps SEE. Unexpectedly, each anti-SEE mediated SEE-induced (CRSwNP), particularly in the subpopulation of patients with aspirin-exacerbated respiratory disease (AERD), as well as those with allergic rhinitis, asthma, and atopic dermatitis.2-5 SAEs are a family of structurally related proteins comprising different From athe Randall Division of Cell and Molecular Biophysics, King’s College London; serological types, such as staphylococcal enterotoxin (SE) A, bthe Genomics Research Center, Academia Sinica, Taipei; cMRC & Asthma UK SEB, SEC, SED, and SEE (up to SEU) and toxic shock syndrome Centre for Allergic Mechanisms of Asthma, King’s College London, Guy’s Campus, toxin 1 (TSST-1).6 SAEs are potent T-cell superantigens, causing London; and dAllergy and Rhinology, Royal National Throat Nose Ear Hospital, London. polyclonal activation of up to 25% of certain T-cell populations Supported by the Medical Research Council (grant no. G1100090), the London Law by interacting with a common b-chain structural framework Trust (to L.K.J.), Medical Research Council (Y.-C.B. Wu), the National Institute for region in the T-cell receptor (TCR),7,8 rather than the Health Research (NIHR) Biomedical Research Centre at Guy’s and St Thomas’ complementarity-determining region (CDR), which recognizes NHS Foundation Trust and King’s College London (to H.J.G., B.J.S., and J.M.M.), and the Wellcome Trust for support of the King’s Biomolecular Spectroscopy Facility specific antigenic peptides bound to MHC. The activity of SEA (085944). The views expressed are those of the authors and not necessarily those of the and SED on B cells in vitro suggests that they can also act as National Health Service, the NIHR, or the Department of Health. B-cell superantigens by binding to the common structural Disclosure of potential conflict of interest: J.-B. Chen has received grants and support for framework regions in the immunoglobulin heavy-chain variable travel to meetings for the study of other purposes from the Genomics Research Center, region (VH) domains shared by immunoglobulins with Academia Sinica. V. J. Lund has received consultancy fees from GlaxoSmithKline, 9-11 Actelion, Vifor, Johnson & Johnson, and Navigent and payment for lectures from different CDRs, as previously shown for staphylococcal 12-14 Neilmed and MSD. The rest of the authors declare that they have no relevant conflicts protein A (SpA). This might increase the polyclonality of of interest. the B-cell repertoire in patients with CRSwNP and allow Received for publication September 25, 2015; revised May 7, 2016; accepted for publi- S aureus to escape immune surveillance.15,16 cation June 13, 2016. Corresponding author: Hannah J. Gould, PhD, Randall Division of Cell and Molecular Nasal polyps in patients with CRSwNP are inflammatory Biophysics, King’s College London, London SE1 1UL, United Kingdom. E-mail: outgrowths of the paranasal sinus mucosa, which are generally [email protected]. characterized by TH2 inflammation, local immunoglobulin 0091-6749 production, and eosinophil infiltration driven by IL-5 and Ó 2016 The Authors. Published by Elsevier Inc. on behalf of the American Academy of eotaxin.17-20 Up to 100% of patients with AERD express Allergy, Asthma & Immunology. This is an open access article under the CC BY li- cense (http://creativecommons.org/licenses/by/4.0/). anti-SAE IgEs in their nasal polyp homogenates and often have http://dx.doi.org/10.1016/j.jaci.2016.06.066 a higher prevalence of comorbid asthma and eosinophilic 1 2 CHEN ET AL J ALLERGY CLIN IMMUNOL nnn 2016 patients with CRSwNP, B cells expressing this IgE are confined Abbreviations used to the nasal mucosa, suggesting a role in sinonasal inflamma- 7-AAD: 7-Aminoactinomycin D tion.17 Whether the SAEs bind to CDRs, framework regions, or AERD: Aspirin-exacerbated respiratory disease both is addressed in the present work. CDR: Complementarity-determining region Antibody production in nasal polyps of patients with CRSwNP: Chronic rhinosinusitis with nasal polyps Fab: Antigen-binding fragment CRSwNP is driven by local activation and differentiation into FACS: Fluorescence-activated cell sorting plasma cells of B cells on exposure to various aeroallergens 26,27 SAE: Staphylococcus aureus enterotoxin and microbial antigens. Thus nasal polyps removed from SE: Staphylococcal enterotoxin patients with AERD provide a unique source of tissue to study SpA: Staphylococcal protein A how SAEs can shape the local antibody repertoire. In the first SPR: Surface plasmon resonance study of this kind, we used an efficient single-cell RT-PCR TCR: T-cell receptor method to clone and express antibodies from single SAE- TSST-1: Toxic shock syndrome toxin 1 specific B cells isolated from the nasal polyps of 3 patients VH: Heavy-chain variable region with AERD and tested their primary function in effector cell VL: Light-chain variable region activation. inflammation,17,21-23 and IgEs from nasal polyps activate 15 METHODS basophils in response to allergens and SEB in vitro. SEB acts Patients’ samples as a human T-cell superantigen in vivo to cause the symptoms 24 Nasal polyps and sera were collected from 3 patients with AERD of atopic dermatitis. Basophils isolated from patients with (HPK-014, HPK-016, and HPK-018) at the Royal National Throat, Nose atopic dermatitis with anti-SAE IgE in their sera, but not those and Ear Hospital, London, United Kingdom. The patients were male, with 25 from healthy control subjects, were responsive to SAEs. a mean age of 56 years. Only patient HPK-014 had positive skin prick Although anti-SAE IgE can be detected in the circulation of test responses to aeroallergens. The ethical committee representing FIG 1. Isolation of SAE1 B cells from nasal polyps by means of FACS. Cells were labeled with a mixture of biotinylated SEA, SED, and SEE and phycoerythrin-coupled anti-CD138, allophycocyanin-coupled anti-CD19, and 7-AAD. A, The lymphocyte population was selected for size and granularity. FSC, Forward scatter; SSC, side scatter. B, Live B cells were identified as CD1917-AAD2 cells. C-E, Fluorescence minus one (FMO) control (Fig 1, C) and no SAE control (Fig 1, D) were used to select SAE1CD191CD13827- AAD2 cells, which constituted 0.25% of the total B-cell population (Fig 1, E). The No SAE control indicates that the cells were stained with all fluorescent antibodies and streptavidin–fluorescein isothiocyanate (FITC) but without biotinylated SAEs, whereas FMO control indicates cells stained with all antibodies but without streptavidin-FITC. J ALLERGY CLIN IMMUNOL CHEN ET AL 3 VOLUME nnn, NUMBER nn FIG 2. Six of the expressed antibodies exhibited SAE binding. The cleared supernatants collected from 293T cells, separately transfected with 40 IgG1 expression plasmids, were tested for reactivity with SEA, SEB, SEC1, SED, SEE, TSST-1, and ovalbumin (OVA) by means of ELISA. An antibody with specificity to a particular SAE was identified with an absolute OD value greater than that of the than control IgG. The antibodies selected for further studies are shown in boldface. Control IgG is a human IgG1 with VH4 and Vk.
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